TcpC inhibits neutrophil extracellular trap formation by enhancing ubiquitination mediated degradation of peptidylarginine deiminase 4

Nat Commun. 2021 Jun 9;12(1):3481. doi: 10.1038/s41467-021-23881-8.

Abstract

TcpC is a multifunctional virulence factor of uropathogenic E. coli (UPEC). Neutrophil extracellular trap formation (NETosis) is a crucial anti-infection mechanism of neutrophils. Here we show the influence of TcpC on NETosis and related mechanisms. We show NETosis in the context of a pyelonephritis mouse model induced by TcpC-secreting wild-type E. coli CFT073 (CFT073wt) and LPS-induced in vitro NETosis with CFT073wt or recombinant TcpC (rTcpC)-treated neutrophils are inhibited. rTcpC enters neutrophils through caveolin-mediated endocytosis and inhibits LPS-induced production of ROS, proinflammatory cytokines and protein but not mRNA levels of peptidylarginine deiminase 4 (PAD4). rTcpC treatment enhances PAD4 ubiquitination and accumulation in proteasomes. Moreover, in vitro ubiquitination kit analyses show that TcpC is a PAD4-targetd E3 ubiquitin-ligase. These data suggest that TcpC inhibits NETosis primarily by serving as an E3 ligase that promotes degradation of PAD4. Our findings provide a novel mechanism underlying TcpC-mediated innate immune evasion.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Chromatin / metabolism
  • Citrullination
  • Escherichia coli Infections / immunology
  • Escherichia coli Infections / pathology
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism*
  • Extracellular Traps / metabolism*
  • Histones / metabolism
  • Immune Evasion
  • Mice
  • Mutation
  • Neutrophils / metabolism*
  • Proteasome Endopeptidase Complex / metabolism
  • Protein-Arginine Deiminase Type 4 / genetics
  • Protein-Arginine Deiminase Type 4 / metabolism*
  • Pyelonephritis / immunology
  • Pyelonephritis / pathology
  • Transcription, Genetic
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism
  • Ubiquitination*
  • Uropathogenic Escherichia coli / metabolism
  • Uropathogenic Escherichia coli / pathogenicity
  • Virulence Factors / genetics
  • Virulence Factors / metabolism*

Substances

  • Chromatin
  • Escherichia coli Proteins
  • Histones
  • TcpC protein, E coli
  • Virulence Factors
  • Ubiquitin-Protein Ligases
  • Proteasome Endopeptidase Complex
  • Protein-Arginine Deiminase Type 4
  • peptidylarginine deiminase 4, mouse